Large-scale interventions may delay decline of the Great Barrier Reef.

On the iconic Great Barrier Reef (GBR), the cumulative impacts of tropical cyclones, marine heatwaves and regular outbreaks of coral-eating crown-of-thorns starfish (CoTS) have severely depleted coral cover. Climate change will further exacerbate this situation over the coming decades unless effective interventions are implemented. Evaluating the efficacy of alternative interventions in a complex system experiencing major cumulative impacts can only be achieved through a systems modelling approach. We have evaluated combinations of interventions using a coral reef meta-community model. The model consisted of a dynamic network of 3753 reefs supporting communities of corals and CoTS connected through ocean larval dispersal, and exposed to changing regimes of tropical cyclones, flood plumes, marine heatwaves and ocean acidification. Interventions included reducing flood plume impacts, expanding control of CoTS populations, stabilizing coral rubble, managing solar radiation and introducing heat-tolerant coral strains. Without intervention, all climate scenarios resulted in precipitous declines in GBR coral cover over the next 50 years. The most effective strategies in delaying decline were combinations that protected coral from both predation (CoTS control) and thermal stress (solar radiation management) deployed at large scale. Successful implementation could expand opportunities for climate action, natural adaptation and socioeconomic adjustment by at least one to two decades.

Interventions to help coral reefs under global change-A complex decision challenge.

Climate change is impacting coral reefs now. Recent pan-tropical bleaching events driven by unprecedented global heat waves have shifted the playing field for coral reef management and policy. While best-practice conventional management remains essential, it may no longer be enough to sustain coral reefs under continued climate change. Nor will climate change mitigation be sufficient on its own. Committed warming and projected reef decline means solutions must involve a portfolio of mitigation, best-practice conventional management and coordinated restoration and adaptation measures involving new and perhaps radical interventions, including local and regional cooling and shading, assisted coral evolution, assisted gene flow, and measures to support and enhance coral recruitment. We propose that proactive research and development to expand the reef management toolbox fast but safely, combined with expedient trialling of promising interventions is now urgently needed, whatever emissions trajectory the world follows. We discuss the challenges and opportunities of embracing new interventions in a race against time, including their risks and uncertainties. Ultimately, solutions to the climate challenge for coral reefs will require consideration of what society wants, what can be achieved technically and economically, and what opportunities we have for action in a rapidly closing window. Finding solutions that work for coral reefs and people will require exceptional levels of coordination of science, management and policy, and open engagement with society. It will also require compromise, because reefs will change under climate change despite our best interventions. We argue that being clear about society's priorities, and understanding both the opportunities and risks that come with an expanded toolset, can help us make the most of a challenging situation. We offer a conceptual model to help reef managers frame decision problems and objectives, and to guide effective strategy choices in the face of complexity and uncertainty.

Spatial resilience of the Great Barrier Reef under cumulative disturbance impacts.

In the face of increasing cumulative effects from human and natural disturbances, sustaining coral reefs will require a deeper understanding of the drivers of coral resilience in space and time. Here we develop a high-resolution, spatially explicit model of coral dynamics on Australia's Great Barrier Reef (GBR). Our model accounts for biological, ecological and environmental processes, as well as spatial variation in water quality and the cumulative effects of coral diseases, bleaching, outbreaks of crown-of-thorns starfish (Acanthaster cf. solaris), and tropical cyclones. Our projections reconstruct coral cover trajectories between 1996 and 2017 over a total reef area of 14,780 km2 , predicting a mean annual coral loss of -0.67%/year mostly due to the impact of cyclones, followed by starfish outbreaks and coral bleaching. Coral growth rate was the highest for outer shelf coral communities characterized by digitate and tabulate Acropora spp. and exposed to low seasonal variations in salinity and sea surface temperature, and the lowest for inner-shelf communities exposed to reduced water quality. We show that coral resilience (defined as the net effect of resistance and recovery following disturbance) was negatively related to the frequency of river plume conditions, and to reef accessibility to a lesser extent. Surprisingly, reef resilience was substantially lower within no-take marine protected areas, however this difference was mostly driven by the effect of water quality. Our model provides a new validated, spatially explicit platform for identifying the reefs that face the greatest risk of biodiversity loss, and those that have the highest chances to persist under increasing disturbance regimes.

The future of resilience-based management in coral reef ecosystems.

Resilience underpins the sustainability of both ecological and social systems. Extensive loss of reef corals following recent mass bleaching events have challenged the notion that support of system resilience is a viable reef management strategy. While resilience-based management (RBM) cannot prevent the damaging effects of major disturbances, such as mass bleaching events, it can support natural processes that promote resistance and recovery. Here, we review the potential of RBM to help sustain coral reefs in the 21st century. We explore the scope for supporting resilience through existing management approaches and emerging technologies and discuss their opportunities and limitations in a changing climate. We argue that for RBM to be effective in a changing world, reef management strategies need to involve both existing and new interventions that together reduce stress, support the fitness of populations and species, and help people and economies to adapt to a highly altered ecosystem.

Contribution of individual rivers to Great Barrier Reef nitrogen exposure with implications for management prioritization.

Dissolved inorganic nitrogen (DIN) runoff from Great Barrier Reef (GBR) catchments is a threat to coral reef health. Several initiatives address this threat, including the Australian Government's Reef 2050 Plan. However, environmental decision makers face an unsolved prioritization challenge: determining the exposure of reefs to DIN from individual rivers. Here, we use virtual river tracers embedded within a GBR-wide hydrodynamic model to resolve the spatial and temporal dynamics of 16 individual river plumes during three wet seasons (2011-2013). We then used in-situ DIN observations to calibrate tracer values, allowing us to estimate the contribution of each river to reef-scale DIN exposure during each season. Results indicate that the Burdekin, Fitzroy, Tully and Daintree rivers pose the greatest DIN exposure risk to coral reefs during the three seasons examined. Results were used to demonstrate a decision support framework that combines reef exposure risk with river dominance (threat diversity).

Impaired recovery of the Great Barrier Reef under cumulative stress.

Corals of the Great Barrier Reef (GBR) have declined over the past 30 years. While reef state depends on the balance between disturbance and recovery, most studies have focused on the effects of disturbance on reef decline. We show that coral recovery rates across the GBR declined by an average of 84% between 1992 and 2010. Recovery was variable: Some key coral types had close to zero recovery by the end of that period, whereas some reefs exhibited high recovery. Our results indicate that coral recovery is sensitive to chronic but manageable pressures, and is suppressed for several years following acute disturbances. Loss of recovery capacity was partly explained by the cumulative effects of chronic pressures including water quality, warming, and sublethal effects of acute disturbances (cyclones, outbreaks of crown-of-thorns starfish, and coral bleaching). Modeled projections indicate that recovery rates can respond rapidly to reductions in acute and chronic stressors, a result that is consistent with fast recovery observed on some reefs in the central and southern GBR since the end of the study period. A combination of local management actions to reduce chronic disturbances and global action to limit the effect of climate change is urgently required to sustain GBR coral cover and diversity.

Vulnerability of the Great Barrier Reef to climate change and local pressures.

Australia's Great Barrier Reef (GBR) is under pressure from a suite of stressors including cyclones, crown-of-thorns starfish (COTS), nutrients from river run-off and warming events that drive mass coral bleaching. Two key questions are: how vulnerable will the GBR be to future environmental scenarios, and to what extent can local management actions lower vulnerability in the face of climate change? To address these questions, we use a simple empirical and mechanistic coral model to explore six scenarios that represent plausible combinations of climate change projections (from four Representative Concentration Pathways, RCPs), cyclones and local stressors. Projections (2017-2050) indicate significant potential for coral recovery in the near-term, relative to current state, followed by climate-driven decline. Under a scenario of unmitigated emissions (RCP8.5) and business-as-usual management of local stressors, mean coral cover on the GBR is predicted to recover over the next decade and then rapidly decline to only 3% by year 2050. In contrast, a scenario of strong carbon mitigation (RCP2.6) and improved water quality, predicts significant coral recovery over the next two decades, followed by a relatively modest climate-driven decline that sustained coral cover above 26% by 2050. In an analysis of the impacts of cumulative stressors on coral cover relative to potential coral cover in the absence of such impacts, we found that GBR-wide reef performance will decline 27%-74% depending on the scenario. Up to 66% of performance loss is attributable to local stressors. The potential for management to reduce vulnerability, measured here as the mean number of years coral cover can be kept above 30%, is spatially variable. Management strategies that alleviate cumulative impacts have the potential to reduce the vulnerability of some midshelf reefs in the central GBR by 83%, but only if combined with strong mitigation of carbon emissions.

Connectivity and systemic resilience of the Great Barrier Reef.

Australia's iconic Great Barrier Reef (GBR) continues to suffer from repeated impacts of cyclones, coral bleaching, and outbreaks of the coral-eating crown-of-thorns starfish (COTS), losing much of its coral cover in the process. This raises the question of the ecosystem's systemic resilience and its ability to rebound after large-scale population loss. Here, we reveal that around 100 reefs of the GBR, or around 3%, have the ideal properties to facilitate recovery of disturbed areas, thereby imparting a level of systemic resilience and aiding its continued recovery. These reefs (1) are highly connected by ocean currents to the wider reef network, (2) have a relatively low risk of exposure to disturbances so that they are likely to provide replenishment when other reefs are depleted, and (3) have an ability to promote recovery of desirable species but are unlikely to either experience or spread COTS outbreaks. The great replenishment potential of these 'robust source reefs', which may supply 47% of the ecosystem in a single dispersal event, emerges from the interaction between oceanographic conditions and geographic location, a process that is likely to be repeated in other reef systems. Such natural resilience of reef systems will become increasingly important as the frequency of disturbances accelerates under climate change.

Joint estimation of crown of thorns (Acanthaster planci) densities on the Great Barrier Reef.

Crown-of-thorns starfish (CoTS; Acanthaster spp.) are an outbreaking pest among many Indo-Pacific coral reefs that cause substantial ecological and economic damage. Despite ongoing CoTS research, there remain critical gaps in observing CoTS populations and accurately estimating their numbers, greatly limiting understanding of the causes and sources of CoTS outbreaks. Here we address two of these gaps by (1) estimating the detectability of adult CoTS on typical underwater visual count (UVC) surveys using covariates and (2) inter-calibrating multiple data sources to estimate CoTS densities within the Cairns sector of the Great Barrier Reef (GBR). We find that, on average, CoTS detectability is high at 0.82 [0.77, 0.87] (median highest posterior density (HPD) and [95% uncertainty intervals]), with CoTS disc width having the greatest influence on detection. Integrating this information with coincident surveys from alternative sampling programs, we estimate CoTS densities in the Cairns sector of the GBR averaged 44 [41, 48] adults per hectare in 2014.

Ocean acidification: Linking science to management solutions using the Great Barrier Reef as a case study.

Coral reefs are one of the most vulnerable ecosystems to ocean acidification. While our understanding of the potential impacts of ocean acidification on coral reef ecosystems is growing, gaps remain that limit our ability to translate scientific knowledge into management action. To guide solution-based research, we review the current knowledge of ocean acidification impacts on coral reefs alongside management needs and priorities. We use the world's largest continuous reef system, Australia's Great Barrier Reef (GBR), as a case study. We integrate scientific knowledge gained from a variety of approaches (e.g., laboratory studies, field observations, and ecosystem modelling) and scales (e.g., cell, organism, ecosystem) that underpin a systems-level understanding of how ocean acidification is likely to impact the GBR and associated goods and services. We then discuss local and regional management options that may be effective to help mitigate the effects of ocean acidification on the GBR, with likely application to other coral reef systems. We develop a research framework for linking solution-based ocean acidification research to practical management options. The framework assists in identifying effective and cost-efficient options for supporting ecosystem resilience. The framework enables on-the-ground OA management to be the focus, while not losing sight of CO2 mitigation as the ultimate solution.

Controlling range expansion in habitat networks by adaptively targeting source populations.

Controlling the spread of invasive species, pests, and pathogens is often logistically limited to interventions that target specific locations at specific periods. However, in complex, highly connected systems, such as marine environments connected by ocean currents, populations spread dynamically in both space and time via transient connectivity links. This results in nondeterministic future distributions of species in which local populations emerge dynamically and concurrently over a large area. The challenge, therefore, is to choose intervention locations that will maximize the effectiveness of the control efforts. We propose a novel method to manage dynamic species invasions and outbreaks that identifies the intervention locations most likely to curtail population expansion by selectively targeting local populations most likely to expand their future range. Critically, at any point during the development of the invasion or outbreak, the method identifies the local intervention that maximizes the long-term benefit across the ecosystem by restricting species' potential to spread. In so doing, the method adaptively selects the intervention targets under dynamically changing circumstances. To illustrate the effectiveness of the method we applied it to controlling the spread of crown-of-thorns starfish (Acanthaster sp.) outbreaks across Australia's Great Barrier Reef. Application of our method resulted in an 18-fold relative improvement in management outcomes compared with a random targeting of reefs in putative starfish control scenarios. Although we focused on applying the method to reducing the spread of an unwanted species, it can also be used to facilitate the spread of desirable species through connectivity networks. For example, the method could be used to select those fragments of habitat most likely to rebuild a population if they were sufficiently well protected.

Operationalizing resilience for adaptive coral reef management under global environmental change.

Cumulative pressures from global climate and ocean change combined with multiple regional and local-scale stressors pose fundamental challenges to coral reef managers worldwide. Understanding how cumulative stressors affect coral reef vulnerability is critical for successful reef conservation now and in the future. In this review, we present the case that strategically managing for increased ecological resilience (capacity for stress resistance and recovery) can reduce coral reef vulnerability (risk of net decline) up to a point. Specifically, we propose an operational framework for identifying effective management levers to enhance resilience and support management decisions that reduce reef vulnerability. Building on a system understanding of biological and ecological processes that drive resilience of coral reefs in different environmental and socio-economic settings, we present an Adaptive Resilience-Based management (ARBM) framework and suggest a set of guidelines for how and where resilience can be enhanced via management interventions. We argue that press-type stressors (pollution, sedimentation, overfishing, ocean warming and acidification) are key threats to coral reef resilience by affecting processes underpinning resistance and recovery, while pulse-type (acute) stressors (e.g. storms, bleaching events, crown-of-thorns starfish outbreaks) increase the demand for resilience. We apply the framework to a set of example problems for Caribbean and Indo-Pacific reefs. A combined strategy of active risk reduction and resilience support is needed, informed by key management objectives, knowledge of reef ecosystem processes and consideration of environmental and social drivers. As climate change and ocean acidification erode the resilience and increase the vulnerability of coral reefs globally, successful adaptive management of coral reefs will become increasingly difficult. Given limited resources, on-the-ground solutions are likely to focus increasingly on actions that support resilience at finer spatial scales, and that are tightly linked to ecosystem goods and services.

Greenhouse conditions induce mineralogical changes and dolomite accumulation in coralline algae on tropical reefs.

Human-induced ocean acidification and warming alter seawater carbonate chemistry reducing the calcification of reef-building crustose coralline algae (CCA), which has implications for reef stability. However, due to the presence of multiple carbonate minerals with different solubilities in seawater, the algal mineralogical responses to changes in carbonate chemistry are poorly understood. Here we demonstrate a 200% increase in dolomite concentration in living CCA under greenhouse conditions of high pCO2 (1,225 µatm) and warming (30 °C). Aragonite, in contrast, increases with lower pCO2 (296 µatm) and low temperature (28 °C). Mineral changes in the surface pigmented skeleton are minor and dolomite and aragonite formation largely occurs in the white crust beneath. Dissolution of high-Mg-calcite and particularly the erosive activities of endolithic algae living inside skeletons play key roles in concentrating dolomite in greenhouse treatments. As oceans acidify and warm in the future, the relative abundance of dolomite in CCA will increase.

INTERACTIONS BETWEEN OCEAN ACIDIFICATION AND WARMING ON THE MORTALITY AND DISSOLUTION OF CORALLINE ALGAE(1).

Coralline algae are among the most sensitive calcifying organisms to ocean acidification as a result of increased atmospheric carbon dioxide (pCO2 ). Little is known, however, about the combined impacts of increased pCO2 , ocean acidification, and sea surface temperature on tissue mortality and skeletal dissolution of coralline algae. To address this issue, we conducted factorial manipulative experiments of elevated CO2 and temperature and examined the consequences on tissue survival and skeletal dissolution of the crustose coralline alga (CCA) Porolithon (=Hydrolithon) onkodes (Heydr.) Foslie (Corallinaceae, Rhodophyta) on the southern Great Barrier Reef (GBR), Australia. We observed that warming amplified the negative effects of high pCO2 on the health of the algae: rates of advanced partial mortality of CCA increased from <1% to 9% under high CO2 (from 400 to 1,100 ppm) and exacerbated to 15% under warming conditions (from 26°C to 29°C). Furthermore, the effect of pCO2 on skeletal dissolution strongly depended on temperature. Dissolution of P. onkodes only occurred in the high-pCO2 treatment and was greater in the warm treatment. Enhanced skeletal dissolution was also associated with a significant increase in the abundance of endolithic algae. Our results demonstrate that P. onkodes is particularly sensitive to ocean acidification under warm conditions, suggesting that previous experiments focused on ocean acidification alone have underestimated the impact of future conditions on coralline algae. Given the central role that coralline algae play within coral reefs, these conclusions have serious ramifications for the integrity of coral-reef ecosystems.

Effects of ocean acidification on microbial community composition of, and oxygen fluxes through, biofilms from the Great Barrier Reef.

Rising anthropogenic CO(2) emissions acidify the oceans, and cause changes to seawater carbon chemistry. Bacterial biofilm communities reflect environmental disturbances and may rapidly respond to ocean acidification. This study investigates community composition and activity responses to experimental ocean acidification in biofilms from the Australian Great Barrier Reef. Natural biofilms grown on glass slides were exposed for 11 d to four controlled pCO(2) concentrations representing the following scenarios: A) pre-industrial (∼300 ppm), B) present-day (∼400 ppm), C) mid century (∼560 ppm) and D) late century (∼1140 ppm). Terminal restriction fragment length polymorphism and clone library analyses of 16S rRNA genes revealed CO(2) -correlated bacterial community shifts between treatments A, B and D. Observed bacterial community shifts were driven by decreases in the relative abundance of Alphaproteobacteria and increases of Flavobacteriales (Bacteroidetes) at increased CO(2) concentrations, indicating pH sensitivity of specific bacterial groups. Elevated pCO(2) (C + D) shifted biofilm algal communities and significantly increased C and N contents, yet O(2) fluxes, measured using in light and dark incubations, remained unchanged. Our findings suggest that bacterial biofilm communities rapidly adapt and reorganize in response to high pCO(2) to maintain activity such as oxygen production.

IMPORTANCE OF MACRO- VERSUS MICROSTRUCTURE IN MODULATING LIGHT LEVELS INSIDE CORAL COLONIES(1).

Adjusting the light exposure and capture of their symbiotic photosynthetic dinoflagellates (genus Symbiodinium Freud.) is central to the success of reef-building corals (order Scleractinia) across high spatio-temporal variation in the light environment of coral reefs. We tested the hypothesis that optical properties of tissues in some coral species can provide light management at the tissue scale comparable to light modulation by colony architecture in other species. We compared within-tissue scalar irradiance in two coral species from the same light habitat but with contrasting colony growth forms: branching Stylophora pistillata and massive Lobophyllia corymbosa. Scalar irradiance at the level of the symbionts (2 mm into the coral tissues) were <10% of ambient irradiance and nearly identical for the two species, despite substantially different light environments at the tissue surface. In S. pistillata, light attenuation (90% relative to ambient) was observed predominantly at the colony level as a result of branch-to-branch self-shading, while in L. corymbosa, near-complete light attenuation (97% relative to ambient) was occurring due to tissue optical properties. The latter could be explained partly by differences in photosynthetic pigment content in the symbiont cells and pigmentation in the coral host tissue. Our results demonstrate that different strategies of light modulation at colony, polyp, and cellular levels by contrasting morphologies are equally effective in achieving favorable irradiances at the level of coral photosymbionts.

High CO2 enhances the competitive strength of seaweeds over corals.

Space competition between corals and seaweeds is an important ecological process underlying coral-reef dynamics. Processes promoting seaweed growth and survival, such as herbivore overfishing and eutrophication, can lead to local reef degradation. Here, we present the case that increasing concentrations of atmospheric CO(2) may be an additional process driving a shift from corals to seaweeds on reefs. Coral (Acropora intermedia) mortality in contact with a common coral-reef seaweed (Lobophora papenfussii) increased two- to threefold between background CO(2) (400 ppm) and highest level projected for late 21st century (1140 ppm). The strong interaction between CO(2) and seaweeds on coral mortality was most likely attributable to a chemical competitive mechanism, as control corals with algal mimics showed no mortality. Our results suggest that coral (Acropora) reefs may become increasingly susceptible to seaweed proliferation under ocean acidification, and processes regulating algal abundance (e.g. herbivory) will play an increasingly important role in maintaining coral abundance.

Heating rate and symbiont productivity are key factors determining thermal stress in the reef-building coral Acropora formosa.

The onset of large-scale coral bleaching events is routinely estimated on the basis of the duration and intensity of thermal anomalies determined as degree heating weeks. Degree heating weeks, however, do not account for differential rates of heating. This study aimed to explore the relationship between different rates of heating above the documented regional winter threshold, and resultant bleaching of the reef-building coral Acropora formosa. Under a relatively low light field, rapid heating of 1 degrees C day(-1) from 29 degrees C to 32 degrees C lead to a 17.6% decline in F(v)/F(m), concurrent with a rapid increase in xanthophyll de-epoxidation sustained into the dark, whereas slower heating rates of 0.5 degrees C day(-1) lead to no decline in F(v)/F(m) and no change in dark-adapted xanthophyll cycling. At the winter bleaching threshold of 30 degrees C, areal net O(2) evolution exceeded the control values for rapidly heated corals, but was lower than the controls for slowly heated corals. At the maximum temperature of 33 degrees C, however, both treatments had net O(2) fluxes that were 50% of control values. At 30 degrees C, only symbiont densities in the slowly heated controls were reduced relative to controls values. By 33 degrees C, however, symbiont densities were 55% less than the controls in both treatments. The rate of heat accumulation was found to be an important variable, with rapidly heated corals attaining the same bleaching status and loss of areal O(2) production for half the degree heating week exposure as slowly heated corals. The study revealed that it is incorrect to assume that significant dark acclimation disables non-photochemical quenching, because 75% of an increased xanthophyll pool was found to be in the de-epoxidated state following rapid heat accumulation. This has important ramifications for the interpretation of chlorophyll fluorescence data such as dark adapted F(v)/F(m).

Making a model meaningful to coral reef managers in a developing nation: a case study of overfishing and rock anchoring in Indonesia.

Most of the world's coral reefs line the coasts of developing nations, where impacts from intense and destructive fishing practices form critical conservation issues for managers. Overfishing of herbivorous fishes can cause phase shifts to macroalgal dominance, and fishers' use of rocks as anchors lowers coral cover, giving further competitive advantage to macroalgae. Overfishing and anchoring have been studied extensively, but the role of their interaction in lowering coral reef resilience has not been quantified formally. We analyzed the combined effects of overfishing and rock anchoring on a range of reef habitat types--varying from high coral and low macroalgae cover to low coral and high macroalgae cover--in a marine park in Indonesia. We parameterized a model of coral and algal dynamics with three intensities of anchoring and fishing pressure. Results of the model indicated that damage caused by rock anchoring was equal to or possibly more devastating to coral reefs in the area than the impact of overfishing. This is an important outcome for local managers, who usually have the funds to distribute less-damaging anchors, but normally are unable to patrol regularly and effectively enough to reduce the impact of overfishing. We translated model results into an interactive visual tool that allows managers to explore the benefits of reducing anchoring frequency and fishing pressure. The potential consequences of inaction were made clear: the likelihood that any of the reef habitats will be dominated in the future by macroalgae rather than corals depends on reducing anchoring frequency, fishing pressure, or both. The tool provides a platform for strengthened relationships between managers and conservationists and can facilitate the uptake of recommendations regarding resource allocation and management actions. Conservation efforts for coral reefs in developing nations are likely to benefit from transforming model projections of habitat condition into tools local managers can understand and interact with.